369 Altitudinal migration in American Dippers (Cinclus mexicanus): Do migrants produce higher quality offspring?
R.H. Mackas, D.J. Green, I.B.J. Whitehorne, E.N. Fairhurst, H.A. Middleton, and C.A. Morrissey
Abstract: Breeding at high elevations can favour life-history strategies in which parents shift to investing in higher quality rather than higher numbers of offspring. In American Dippers (Cinclus mexicanus Swainson, 1827), altitudinal migrants produce fewer fledglings than sedentary individuals (residents) that breed at lower elevations. We examined whether mi- grants compensate for their lower fecundity by providing their offspring with a higher quality diet and (or) more food, and producing higher quality offspring. Nestling diet was assessed using observations and stable isotope analysis of feathers grown during the nestling period. Nestling quality was assessed using a condition index (residuals from a mass–tarsus re- gression) and postfledging survival. We found that migrants fed their offspring less fish, and despite having higher feeding rates, had lower energetic provisioning rates than residents. Migrants also produced offspring that were in worse condition and had lower postfledging survival. This study found no evidence that altitudinal migration is associated with a trade-off favouring the production of smaller numbers of higher quality young. Instead our data provide support for the hypothesis that altitudinal migration in American Dippers is an outcome of competition for limited nest sites at lower elevations that forces some individuals to move to higher elevations to breed. Re´sume´ : La reproduction aux hautes altitudes peut favoriser des strate´gies de´mographiques dans lesquelles les parents in- vestissent dans des rejetons de plus grande qualite´ plutoˆt que dans un nombre plus e´leve´ de rejetons. Chez le cincle d’Ame´rique (Cinclus mexicanus Swainson, 1827), les individus qui migrent en altitude produisent moins de petits a` l’envol que les individus se´dentaires (re´sidants) des altitudes plus basses. Nous ve´rifions si les migrateurs compensent leur fe´con- dite´ re´duite en procurant a` leurs rejetons un meilleur re´gime alimentaire ou un re´gime plus abondant et en produisant ainsi des petits de meilleure qualite´.Lere´gime alimentaire des petits au nid a pu eˆtre de´termine´ par observation directe et par analyse des isotopes stables dans les plumes e´labore´es durant la pe´riode au nid. La qualite´ des petits au nid a e´te´ mesure´e par un indice de condition (re´sidus de la re´gression de la masse sur le tarse) et par la survie apre`s l’envol. Les migrateurs apportent moins de poissons a` leurs rejetons et, malgre´ des taux d’alimentation plus e´leve´s, ils ont des taux d’approvision- nement en e´nergie infe´rieurs a` ceux des re´sidants. Les migrateurs produisent aussi des petits en moins bonne condition dont la survie apre`s l’envol est infe´rieure. Notre e´tude n’offre aucune indication que la migration en altitude comporte un compromis favorisant la production de petits moins nombreux mais de meilleure qualite´. Au contraire, nos donne´es ap- puient l’hypothe`se selon laquelle la migration en altitude chez les cincles d’Ame´rique re´sulte de la compe´tition pour un nombre limite´ de sites de nidification aux altitudes infe´rieures, ce qui oblige certains individus a` se de´placer vers les altitu- des supe´rieures pour leur reproduction. [Traduit par la Re´daction]
Introduction dinal migration may be advantageous because it allows mi- grants to exploit temporal or spatial variation in food Altitudinal migration is a common strategy of birds occupy- resources (Loiselle and Blake 1991; Solo´rzano et al. 2000), ing mountainous habitat but has been studied less intensively minimize the risk of nest predation (Boyle 2008; Fretwell than latitudinal migration (Berthold 2001; Newton 2008). For 1980), or escape extreme climatic conditions that impact phys- most altitudinal migrants seasonal movements are relatively iological function (Cox 1985). short and involve migrating uphill to breeding areas and Seasonal movements to higher elevation breeding sites can downhill to nonbreeding areas (Burgess and Mlingwa 2000; impose selection pressures that lead to elevation-specific life- Dingle 2004; Johnson and Maclean 1994; Stiles 1983). Altitu- history strategies. For example, a comparison of phylogeneti-
Received 11 November 2009. Accepted 11 February 2010. Published on the NRC Research Press Web site at cjz.nrc.ca on 10 March 2010. R.H. Mackas, D.J. Green,1 I.B.J. Whitehorne, E.N. Fairhurst,2 H.A. Middleton, and C.A. Morrissey.3 Centre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada. 1Corresponding author (e-mail: [email protected]). 2Present address: Department of Biology, Dalhousie University, Halifax, NS B3H 4J1, Canada. 3Present address: School of Biosciences, Cardiff University, Cardiff, UK.
Can. J. Zool. 88: 369–377 (2010) doi:10.1139/Z10-013 Published by NRC Research Press 370 Can. J. Zool. Vol. 88, 2010 cally paired avian taxa from low- and high-elevation sites in- and mountain streams. Dippers construct large domed nests dicates that high-elevation species have smaller clutches and 1–5 m above the water on cliff ledges, boulders, the ends of fewer broods per year than their low-elevation counterparts overhanging logs, in undercut banks, and on bridges (Badyaev and Ghalambor 2001). Badyaev and Ghalambor (Kingery 1996). Although both sexes contribute to territory (2001) found that the reduced fecundity in these high- defence, nest building, and the care of nestlings and fledg- elevation species is associated with increased parental care lings, only females incubate eggs and brood young. Dippers and a shift away from investment in offspring number toward will typically renest if a clutch or brood is lost early in the investment in offspring quality. Similar life-history trade-offs breeding season and may raise up to two broods per season have been described within species that breed on a steep- (Gillis et al. 2008; Kingery 1996; Price and Bock 1983). elevation gradient. For example, Dark-eyed Juncos (Junco We have studied an individually marked population of hyemalis (L., 1758)) that breed at high elevations initiate American Dippers in the Chilliwack River watershed, lo- breeding later and have a more compressed breeding season cated in the Cascade Mountain Range of southwestern Brit- than Dark-eyed Juncos breeding at low elevations, and conse- ish Columbia, Canada, from 1999 to 2009. This population quently produce fewer broods and fledglings per season. is composed of both altitudinal migrants and sedentary indi- However, Dark-eyed Juncos at high elevations produce heav- viduals (residents); approximately 85% of individuals are al- ier offspring with greater fat reserves than Dark-eyed Juncos titudinal migrants (Morrissey et al. 2004a). Adults rarely at low elevations (Bears et al. 2009). switch from being migratory to sedentary or vice versa, but Most populations of American Dippers (Cinclus mexicanus individuals frequently adopt a different strategy to their pa- Swainson, 1827) contain altitudinal migrants, individuals that rents (Gillis et al. 2008). Migrants overwinter with residents move between winter habitat on the coast or on rivers at low on the main stem of the Chilliwack River but move to elevations and breeding habitat on higher elevation streams higher elevation breeding sites on first- to third-order (Morrissey et al. 2004a; Price and Bock 1983; Willson and streams in the spring (February–April). On average, mi- Hocker 2008). Some populations contain both migratory and grants travel 6 km (range 2–21 km) and gain a mean of sedentary individuals, allowing the life-history consequences 226 m (range 10–735 m) as they move to higher elevation of altitudinal migration to be compared in a single population. territories in the breeding season (n = 33 birds; D.J. Green, In British Columbia, Canada, migrants consistently have unpublished data). Migrants have lower productivity (2.3 vs. lower productivity than residents because they initiate breed- 3.7 fledglings/year) but have higher annual survival (57.3% ing later and are consequently less likely to raise a second vs. 53.9%) than residents (Gillis et al. 2008). brood (Gillis et al. 2008; Morrissey 2004). Migrants, how- ever, have higher annual adult survival than residents (Gillis Monitoring reproduction and estimating nestling et al. 2008). Gillis et al. (2008) argued that migrants were condition making the ‘‘best of a bad job’’ when moving to higher eleva- tion breeding habitat, as the difference in adult survival was Breeding pairs were located by searching accessible sec- not sufficient to offset the lower productivity and the lifetime tions of the river and higher elevation creeks on foot, check- reproductive success of migrants was predicted to be lower ing suitable locations for nests, and following any dippers than that of residents. This argument, however, ignores the seen or heard. Breeding pairs were classed as sedentary if possibility that migrants in addition to having higher annual they occupied breeding territories on or within 1 km of the survival as adults may also compensate for their reduced fe- main stem of the Chilliwack River and were observed in the cundity by producing offspring of higher quality. same area during fall and winter. Pairs were classified as In this paper we assess whether breeding at higher eleva- migrants if they occupied breeding territories on creeks tions can lead to a shift in the life-history strategies of Amer- more than 1 km from the main stem of the river and were ican Dippers favouring the production of higher quality not observed on these territories in winter. Where possible rather than higher numbers of offspring. We assess whether nests were checked every 3–7 days to determine clutch ini- the seasonal movement of migrants enables them to exploit tiation dates, hatch dates, clutch and brood sizes, and the different prey and (or) provision at a higher rate than resi- fate of all nesting attempts. Precise hatch dates were calcu- dents using a combination of feeding observations, estimates lated using the nestling age at the first nest check after of energetic provisioning rates, and stable isotope analysis of hatching. Brood size and the mean nestling condition index juvenile feathers grown during the nestling period. Aquatic for each brood were determined when nestlings were larval invertebrates are the principal prey fed to nestling dip- banded, weighed, and measured 10–15 days (12.4 ± pers, but small fish are an alternative prey with higher ener- 2.0 days; mean ± SD) after hatching. The condition index getic content and nutritional value (Obermeyer et al. 2006). for each nestling was estimated using the residual from a We also examine whether differences in diet quality or provi- tarsus length – body mass regression. We were unable to es- sioning rate allow migratory dippers to compensate for their timate chick growth rates because of logistic difficulties as- lower annual fecundity by producing offspring that are in sociated with removing nestlings from nests located on cliffs better condition and (or) have higher postfledging survival. or bridges over fast-flowing rivers or streams multiple times. When nests were inaccessible, hatch dates were estimated Materials and methods by backdating from the date the brood fledged assuming that fledging occurs 25 days after hatching (Price and Bock Study species and site 1983). Brood size at these nests was assumed to equal the American dippers are aquatic passerines that feed on number of fledglings observed during thorough searches of freshwater invertebrates and small fish in fast-flowing rivers the territory within 2 days of fledging.
Published by NRC Research Press Mackas et al. 371
Feeding observations isotope analysis. Invertebrate samples, which were a composite We conducted feeding observations at 68 nests between of prey collected at each site, were rinsed with deionized water 2005 and 2008 (2005: n = 7; 2006: n = 22; 2007: n = 18; and oven dried at 40 8C for 48 h. Fish samples were rinsed with 2008: n = 21). Observations were conducted throughout the deionized water and freeze-dried for 48 h. Each fish and inver- day and varied in length from 30 to 200 min (66 ± 34 min; tebrate sample was then ground into homogenous powder and mean ± SD). All nests were observed midway through the subsamples of approximately 1 mg from each fish or inverte- nestling period when nestlings were 8–14 days of age, and brate sample were measured into miniature tin capsules 23 nests were also observed a second time late in the nestling (Costech Analytical Technologies, Inc., Valencia, California, period when nestlings were 17–24 days of age. During obser- USA) for isotopic analysis. vation periods we recorded when parents delivered food to We collected feather samples (the innermost right primary) the nest and the prey type and load size of each delivery. from a total of 63 juvenile dippers from 20 broods produced in Prey items were classified as aquatic invertebrates, fish eggs, 2008. Samples came from nestlings aged 11–14 days or re- and small fish. Deliveries of aquatic invertebrates were not cently fledged juveniles aged 25–40 days captured in mist defined more precisely because deliveries often include mul- nets set up across small channels in the natal territory. We pre- tiple prey taxa and we were often unable to identify the taxa pared feather samples for stable isotope analysis by removing being delivered. However, load sizes were classified as being the sheath from feathers that were not completely emerged, small, medium-sized, or large and were estimated in relation washing all feathers in a 2:1 chloroform and methanol solu- to the size of the bill. We subsequently grouped deliveries tion for 48 h, and air-drying them for a further 48 h. Samples into seven categories (Table 1). of approximately 1 mg were cut from the distal tip of each feather, weighed, and transferred into miniature tin capsules Prey and feather sampling for isotopic analysis. Prey and feather samples were collected so that we could (i) determine the mass and energetic content of the seven cat- Stable isotope analysis egories of food delivered to the nest and (ii) determine the Stable isotope ratios of nitrogen in the feather and prey stable isotope signatures of prey and feathers needed to calcu- samples were analysed at the Stable Isotope Facility, late the proportion of invertebrates and fish in the diet of University of California Davis, Davis, California, USA, using nestlings. We obtained larval aquatic invertebrate samples a PDZ Europa ANCA-GSL elemental analyzer interfaced to from six sites on the Chilliwack River and five sites on four a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon higher elevation creeks in 2008 by turning over rocks and Ltd., Cheshire, UK). Sample nitrogen isotope ratios were collecting all macroinvertebrates >2 mm long by hand. Each compared with those in air. Values for 15N were calculated sample included plectopteran and ephemopteran nymphs and and reported using the standard delta (d) notation in parts per trichopteran larvae, all of which are preyed on by dippers thousand (%). During analysis, samples were interspersed (Bakus 1959; Mitchell 1968). Samples of salmonid fry were with replicate laboratory standards that had been previously collected from the Chilliwack River and three creeks using a calibrated against NIST Standard Reference Materials dip net. We targeted fish of the size observed during (IAEA-N1, IAEA-N2, IAEA-N3, IAEA-CH7, and NBS-22). provisioning observations (~40 mm long). All fish sampled Measurement error was ±0.1%. were either coho salmon (Oncorhynchus kisutch (Walbaum, 1792)) or steelhead (Oncorhynchus mykiss (Walbaum, 1792)). Invertebrate and fish samples were stored in ethanol prior to Postfledging survival being transferred to the laboratory. We examined the postfledging survival of all banded nest- We calculated the energetic value of small, medium-sized, lings known to have fledged between 1999 and 2008 (n = and large invertebrate deliveries by preparing 11 prey sub- 526). Survival from fledging until the end of January the samples representative of each load size, determining their following year was assessed using resighting data obtained dry mass, and converting these mass to energetic values during systematic censuses of the Chilliwack River conducted using published values for aquatic invertebrates (Table 1). five times a year between November 1999 and July 2009, Invertebrate subsamples contained multiple prey with individ- detailed searches of the main stem of the river and higher ele- uals from each major taxa being combined to create load sizes vation tributaries conducted each breeding season (2000– that approximated invertebrate deliveries made by dippers, 2009), and regular visits to the study area made to capture using tweezers with marks corresponding to 1/4, 1/2, and 1 and mark breeding and wintering adults (for more details see dipper bill length as a reference. Invertebrate subsamples Gillis et al. 2008). Our use of juvenile survival to assess the were rinsed with deionized water and oven dried at 40 8C for quality of offspring raised by migrants and residents could be approximately 48 h prior to weighing. We estimated the ener- biased if the offspring of migrants disperse farther, are more getic content of fish or steelhead eggs delivered to nestlings likely to disperse outside the watershed, and are less likely to using published data on the size–mass relationship and ener- be detected. However, we believe that any resighting bias is getic content for juvenile salmon or salmonid eggs (Table 1). likely to be small because the offspring of migrants Fish fed to nestlings were approximately twice the bill length overwinter with the offspring of residents on the main stem of an adult dipper, so fish were assumed to be 44 mm long. of the river, the migratory strategy of an individual cannot be Energetic values for the different prey types and load sizes predicted by the strategy of their parents, and the distance were then used to calculate the energetic provisioning rate from the natal territory to the point individuals are resighted (kJ/h) during each provisioning observation. is small compared with the length of the study area (Gillis et We also prepared invertebrate and fish samples for stable al. 2008; Middleton and Green 2008).
Published by NRC Research Press 372 Can. J. Zool. Vol. 88, 2010
Data analysis We conducted a total of 91 provisioning observations at 68 nests containing broods produced by 54 pairs and deter- mined the mean nestling condition of 59 broods produced by 34 pairs. We therefore used a mixed modeling approach to test whether migrants provide their offspring with a higher quality diet, deliver food at a higher rate, and produce higher quality offspring than residents. We examined five independent variables: the proportion of deliveries that con- (fish and invertebrates) 7.21 6.82 tained fish, whether at least one fish was delivered during a ) broods. provisioning observations (yes or no), the delivery rate of both parents (total number of feeding visits/h), the energetic
delivery. The references give estimates for provisioning rate (kJ/h), and the average nestling condition of a brood. Pair identity was included as a random term in { all models. We included six explanatory variables in each (fish) 4.40 — 1.11 model: migratory strategy, hatch date, year, brood-size cate-
Cinclus mexicanus gory (small = 1 or 2; medium-sized = 3; large = 4 or 5), nestling age, and the time of day observations were con- ducted (morning 0800–1200; midday 1200–1600; afternoon 1600–2000). Brood size was categorized as a factor with three levels, as brood sizes of 1 and 5 were rare. For each analysis, we initially fitted a full model including all main || (invertebrates) effects and interaction terms, and then sequentially elimi- Energetic content 22.9 —7.8 4.40 nated all nonsignificant interactions and then main effects until only significant terms remained. To ensure that the or- der in which terms were dropped did not influence the final model selected, we re-evaluated any term eliminated by add-
{ § ing and dropping it from the final reported model. We as-
(fish) sessed the significance of terms in models by using the 1.55 change in deviance or the Wald statistic associated with dropping individual terms from models. Both the change in deviance and the Wald statistic approximate a c2 distribu- tion. Estimates of effects and predicted means are presented with standard errors. We used generalized linear mixed models (GLMM) to in-
(invertebrates) vestigate how nestling condition and the migratory strategy 0.017 (altitudinal migrant or resident) of their parents influenced the postfledging survival of 526 fledglings produced by 104 pairs. Pair identity was included as a random term. Models were fitted to examine the relationship between survival and migratory strategy, survival and nestling condition, and survival and migratory strategy after controlling for nestling condition, year, and hatch date. Significance of explanatory terms was evaluated using the Wald statistic. All models were fitted using GenStat version 11 (VSN International
bill length 0.169 — 22.9Ltd., Hemel Hempstead, — UK). 3.87 bill length (invertebrates) bill length 0.017 — 22.9* — 0.39